Introduction 1999 Lissamphibia Amphibia 1985 2003 Archaeobatrachia Neobatrachia 1985 1990 2005 1985 1 2006 In mammals, the mechanical tuning of the basilar membrane is the primary basis for frequency selectivity. In the absence of the basilar membrane, the frog’s auditory organs must rely solely on the tectorial membrane and on the hair cells themselves for frequency selectivity. 2007 1999 2000a Anatomy Middle ear 2 tympanic annulus 1998 2002a 1988 2003 1998 2002b An additional bony disk, the operculum, is flexibly attached to the oval window in amphibians. The presence of an operculum in anurans is unique among vertebrates. The operculum’s position in the oval window can be modulated through the m. opercularis, which also connects it to the shoulder girdle. 1999 2002b 1988 1985 1985 2002b 1988 Ranidae Xenopus leavis 1985 Telmatobius exsul 1988 Bombina 1999 1985 Bombina bombina 1988 Atelopus 1998 1988 1988 1998 1999 Inner ear 2000a 1 2000b Fig. 1 1985  colored arrows  green arrows  red arrows  blue arrows  grey areas  dark yellow  green areas  1999 1985 three cristae in the semi-circular canals, which are sensitive to rotational acceleration of the head, the utricule, which detects linear acceleration, 1977 1990 1991 1975 1975 1988 2000 2006 2003 3 Basilar papilla 1999 1985 Rana catesbeiana 1957 Rana pipiens pipiens 1985 Rana catesbeiana 1985 Ranidae 1974 1985 1999 4 Amphibian papilla The amphibian papilla can be found in a recess, that extends medially from the saccular space and, in frogs with derived ears, bends caudally to end at a contact membrane. Like the basilar papilla’s contact membrane, the membrane separates the endolymphatic fluid in the papilla recess from the perilymphatic fluid at the round window. 1999 2 Ranidae 1984 1981 Fig. 2 Rana catesbeiana 1982 1  TM  AP  a  dashed outline  b  dashed line  2 1981 1982 1983 1985 1990 1982 Response of the auditory end organs Anatomy 2000a 2000b 2000b 2000a 3 2000b Fig. 3 Rana left Hyla right  dashed lines  a  b Rana pipiens pipiens Hyla cinerea c R. catesbeiana  black line  open markers  d e R. pipiens pipiens R. esculenta H. cinerea H. chrysoscelis H. versicolor f R. pipiens pipiens g  h Rana pipiens pipiens Hyla cinerea  a  b  d e g  h 2006 1990 1983 1989 1996 2004 2001  c 2000a  f 2006  2000a Basilar papilla The basilar papilla’s tectorial membrane is presumably driven by a vibrating pressure gradient between the the sacculus and the basilar papilla’s contact membrane. No reports have been published on direct measurements of the mechanical response of the tectorial membrane, or on the basilar papilla’s hair bundle mechanics. However, the hair cell orientation in the basilar papilla implies that the tectorial membrane’s primary mode of motion is to and from the sacculus. 4 1990 1981 1991 Hyla Hyla cinerea 1980 1983 Hyla regilla 1990 1991 Scaphiopus couchi 1975 1991 Eleutherodactylus coqui 1980 1976 1991 Physalaemus pustulosus 2001 Fig. 4 R. catesbeiana \documentclass[12pt]{minimal}
\usepackage{amsmath}
\usepackage{wasysym} 
\usepackage{amsfonts} 
\usepackage{amssymb} 
\usepackage{amsbsy}
\usepackage{mathrsfs}
\usepackage{upgreek}
\setlength{\oddsidemargin}{-69pt}
\begin{document}$$Q_{10{\rm dB}}$$\end{document}  1990 2006 1988 Q dB 1976 1981 1975 5 1991 5 Hyla regilla Scaphiopus couchi Fig. 5 \documentclass[12pt]{minimal}
\usepackage{amsmath}
\usepackage{wasysym} 
\usepackage{amsfonts} 
\usepackage{amssymb} 
\usepackage{amsbsy}
\usepackage{mathrsfs}
\usepackage{upgreek}
\setlength{\oddsidemargin}{-69pt}
\begin{document}$$Q_{10{\rm dB}}$$\end{document} 1975 1991  triangular symbols  circles   black line  grey area  upper  lower  loops  lower   3 2001 2006 2003 2004 2005 2006 2007 2001 1982 2006 2005 2005 1957 Amphibian papilla As in the basilar papilla, the tectorial membrane in the amphibian papilla is presumably driven by a vibrating pressure difference between the sacculus and the round window. Due to the more elaborate tectorial membrane and the more complex pattern of hair cell orientations, the motion of the membrane may be expected to be more complex than that of the basilar papilla’s tectorial membrane. The tectorial curtain is in the sound path through the papilla, and presumably plays a role in conveying vibrations to the tectorial membrane and the hair bundles. 1982 2 5 1990 1975 5 1987 1999 1987 1984 1980 1994 1994 1997 2004 2000 2 1989 1996 1996 2001 3 2001 2004 2006 2003 1996 2006 Discussion 2000a The amphibian and the basilar papilla are the only hearing organs found in terrestrial vertebrates in which the hair cells are not on a flexible basilar membrane. Instead the hair cells are embedded in a relatively stiff cartilaginous support structure. Any frequency selective response, therefore, most likely originates from the mechanical or electrical properties of the hair cells, or the mechanical properties of the tectorial membrane, or a combination of these factors. Since there are no direct mechanical measurements of either the hair cells in the papillae or the tectorial membranes, we cannot come to any definite conclusions regarding their properties. However, the available morphological and functional data allow for some hypotheses. 1982 1987 1984 1999 1981 the papilla is elongated, and it exhibits a tonotopic gradient along the long axis; the orientation of the hair cells is perpendicular to the tonotopic axis, indicating that the hair cells are stimulated most efficiently by a deflection perpendicular to the tonotopic axis; frequency selectivity, very probably, relies on mechanical tuning; Q dB both spontaneous and distortion product otoacoustic emissions are generated. These emissions are physiologically vulnerable. 1999 1985 2000 2000 2002 2003 1999 2003 2003 2000 The basilar papilla seems to function in a much simpler manner. Both neural recordings and otoacoustic emission measurements suggest that it functions as a single auditory filter. Since the hair cells in the basilar papilla are unlikely to be electrically tuned, its frequency selectivity most likely results from mechanical tuning, probably via the tectorial membrane. 2001 2006 2003 2004 2006 In conclusion, the frog inner ear takes an exceptional place among the hearing organs of terrestrial vertebrates. It includes two auditory end organs, which both lack the basilar membrane present in every other terrestrial vertebrate species. Instead the hair cells are embedded in a relatively stiff structure. They are stimulated by the motion of the tectorial membrane. Although the basilar and amphibian papilla are similar in this respect, they appear to function by different mechanisms. In fact, even within the amphibian papilla two distinctly different functional regions can be identified. The low-frequency portion, rostral to the tectorial curtain, contains hair cells that exhibit electrical tuning. The hair cells are most sensitive to deflection along the tonotopic axis, thus this is presumably the tectorial membrane’s direction of vibration. By contrast, the region caudal to the tectorial curtain shows more similarities to, for example, the mammalian cochlea: the hair cell orientation is perpendicular to the tonotopic axis, and the presence of spontaneous otoacoustic emissions suggests that it functions as an active hearing organ. Finally, the basilar papilla is yet different: it appears to function as a single passive auditory filter. Thus the frog inner ear includes two auditory end organs with three functional regions.